Journal of Experimental Biology • Accepted Manuscript Summary Statement

Run and hide: visual performance in a brittle star Lauren Sumner-Rooney1*, John D Kirwan2, Carsten Lüter3, Esther Ullrich-Lüter3 1Oxford University Museum of Natural History, University of Oxford, Parks Road, Oxford OX1 3PW, UK. 2Stazione Zoologica Anton Dohrn, Via Francesco Caracciolo, 333, 80122 Naples, Italy. 3Museum für Naturkunde, Leibniz Institute for Evolution and Biodiversity, Invalidenstrasse 43, 10115 Berlin, Germany. *Corresponding author: [email protected] Key words: Echinoderms, extraocular vision, ophiuroids, vision © 2021. Published by The Company of Biologists Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed. Journal of Experimental Biology • Accepted manuscript Summary statement Sumner-Rooney et al. characterise responses to static visual stimuli of varying size and contrast, as well as to moving shadows, in a brittle star. Abstract Spatial vision was recently reported in a brittle star, Ophiomastix wendtii, which lacks discrete eyes, but little is known about its visual ecology. Our aim was to better characterize the vision and visual ecology of this unusual visual system. We tested animals’ orientation relative to vertical bar stimuli at a range of angular widths and contrast, to identify limits of angular and contrast detection. We also presented dynamic shadow stimuli, either looming towards or passing overhead the animal, to test for potential defensive responses. Finally, we presented animals lacking a single arm with a vertical bar stimulus known to elicit a response in intact animals. We found that O. wendtii orients to large (≥50°), high-contrast vertical bar stimuli, consistent with a shelter-seeking role and with photoreceptor acceptance angles estimated from morphology. We calculate poor optical sensitivity for individual photoreceptors, and predict dramatic oversampling for photoreceptor arrays. We also report responses to dark stimuli moving against a bright background - this is the first report of responses to moving stimuli in brittle stars and suggests additional defensive uses for vision in echinoderms. Finally, we found that animals missing a single arm orient worse to static stimuli, which requires further investigation. Journal of Experimental Biology • Accepted manuscript Introduction Light is a critical biological cue, and detecting it can play a role in habitat selection, defensive behaviour, UV protection, and biological rhythms. Image-forming vision can facilitate more complex behaviours including navigation, communication and pursuit (Nilsson, 2013). Eyes – discrete sensory organs that facilitate vision – have evolved dozens of times among animals and exhibit a stunning diversity of forms (Land and Nilsson, 2012; von Salvini-Plawen and Mayr, 1977). Many animals also detect light using extraocular photoreceptors, in the brain, skin, in intrinsically light-sensitive neurons, or elsewhere (e.g. Battelle, 2016; Kingston and Cronin, 2016; Ramirez et al., 2011; Tong et al., 2009). Until recently, it was considered that these extraocular photoreceptors did not contribute to vision or visual processes (reviewed in Cronin and Johnsen, 2016). Recent experiments evince extraocular photoreceptors mediating vision in echinoderms (Blevins and Johnsen, 2004; Kirwan et al., 2018; Sumner-Rooney et al., 2020; Yerramilli and Johnsen, 2010). In both sea urchins (Ullrich-Lüter et al., 2011) and brittle stars (Delroisse et al., 2014; Johnsen, 1997; Sumner-Rooney et al., 2018), putative photoreceptors are spread over the body surface, and in select species these appear to mediate responses to visual stimuli, undetectable by non-visual photoreception (Kirwan et al., 2018; Sumner-Rooney et al., 2020). The occurrence of extraocular vision in at least two classes of echinoderms opens up a host of new questions and potential research avenues concerning their function, limitations, signal integration, and evolution. Our fundamental understanding of vision has been built on centuries of work on animal eyes. Distributed visual systems, including those of ark clams and fan worms (Nilsson, 1994), break from many of the conventions of paired eyes, but still retain discrete visual units. Extraocular systems, however, cannot be easily described optically because photoreceptors are not arranged in adjacent rows within a discrete structure, making properties such as acceptance angle more difficult to estimate. These animals therefore represent a challenge for visual biologists. With a better understanding of extraocular visual systems and their capabilities, we may also find new resources Journal of Experimental Biology • Accepted manuscript and inspiration for biomimetic sensor technology (e.g. Aizenberg and Hendler, 2004; Mao et al., 2013; Watanabe et al., 2011; Yang and Aizenberg, 2005). The brittle star Ophiomastix wendtii (Müller and Troschel, 1842; formerly Ophiocoma wendtii, according to O’Hara et al., 2019) orients to isoreflectant stimuli. These reflect the same amount of light, in total, as the background against which they are presented, and are therefore detectable only via object resolving vision (Sumner-Rooney et al., 2020). Ophiomastix wendtii inhabits densely populated reef rubble in the Caribbean and Gulf of Mexico, where predation pressure is high. Parrotfish, wrasse and mojarra are all reported to feed on members of the genus, with the greatest threat from Sparisoma and Halichoeres spp. (Hendler, 1984). These are large, fast-moving diurnal species that are present in high numbers and particularly parrotfish and mojarra may consume whole animals (Hendler, 1984). Orientation to these static stimuli may reflect motivation to seek shelter in bright, heterogenous reef rubble habitats, and that animals are attracted to regions of local contrast that might indicate structural heterogeneity and therefore potential refuge from predation (Sides and Woodley, 1985). Clarifying the visual acuity exhibited by Ophiomastix would shed light on both visual function and visual ecology in relation to this behaviour; for example, Sides and Woodley (1985) suggested that O. wendtii maintained sympatry with other ophiocomids by selecting larger crevices in which to shelter. This could reflect a limit on acuity or a selective preference. Moreover, high contrast signals (as used by Sumner-Rooney et al., 2020) are uncommon in oceanic water, and investigating contrast sensitivity at detectable spatial frequencies (once identified) helps infer how performance and visual ecology interrelate. Although the habitat of O. wendtii is shallow and bright, we might expect animals to respond to lower contrast signals more representative of natural scenes if this behaviour is biologically relevant. Journal of Experimental Biology • Accepted manuscript Other uses for low-resolution vision may exist, besides habitat selection. To date, only static stimuli have been tested in Ophiomastix, but their natural visual environment is busy and dynamic. Responses to moving stimuli might reveal additional or alternative roles of vision in predator detection. In Diadema, both the sudden and looming appearance of dark stimuli against a bright background elicited a characteristic defensive spine-pointing response. In other distributed visual systems, including chiton shell eyes, ark clam compound eyes and fanworm radiolar eyes, predator detection is the core task of vision (Bok et al., 2019; Nilsson, 1994; Speiser et al., 2011). Other than arm autotomy, defensive or harm-reductive behaviours are not extensively documented in brittle stars. Hendler (1984) reported that arm spines would raise and lock into place and that animals produce mucus when they are mechanically disturbed. The nocturnal activity patterns and proposed shelter-seeking of O. wendtii may contribute to their avoidance of predation, but given their vulnerability to fast-moving visual predators during the day, we might expect them to respond to moving shadows. How animals might integrate information from thousands of dispersed photoreceptors remains uncertain. Sumner-Rooney et al. (2020) highlighted a distinction in locomotion between sighted Ophiomastix and a closely related but apparently non-sighted species Ophiocomella pumila (Lütken, 1856), which they proposed was a possible clue to signal integration. Leading with a single arm (“rowing”; Astley, 2012) appears to be the dominant locomotory mode in most ophiuroid species studied to date (Arshavskii et al., 1976; Astley, 2012; Clark et al., 2018; Glaser, 1907; Wakita et al., 2020). “Reverse rowing” (Astley, 2012), with two leading arms, is also widely reported but seems to be less common. While O. pumila almost always moved by rowing, O. wendtii used reverse rowing in the majority of experiments (Sumner-Rooney et al., 2020). These authors suggested that leading with two outstretched arms could indicate signal comparison between them in O. wendtii; the complex and variable body shape and relatively rapid movement of Ophiomastix likely presents significant additional challenges for extraocular vision in comparison to the fixed spherical shape of sea urchins. Comparing pooled photoreceptor signal between adjacent arms could be a much Journal of Experimental Biology • Accepted manuscript simpler method of contrast detection than integrating spatial signal within arms or across the whole

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